Journal of Ecology ( IF 5.3 ) Pub Date : 2022-07-08 , DOI: 10.1111/1365-2745.13964 Carlos M. Herrera 1 , Mónica Medrano 1 , Pilar Bazaga 1 , Conchita Alonso 1
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1 INTRODUCTION
The notion that individual plants are nonunitary entities can be traced back at least to the work of Erasmus Darwin (1800), who emphasized that ‘…every bud of a tree is an individual vegetable being; and that a tree therefore is a family or swarm of individual plants’. In more recent times, the ecological, evolutionary and physiological implications of the internal multiplicity inherent to modular plant growth have been examined in considerable detail from different perspectives and with reference to a variety of subindividual units (Herrera, 2009). These latter include, for instance, physiologically autonomous sectors (Orians & Jones, 2001; Watson, 1986; Watson & Casper, 1984), branches and ortostichies (Orians et al., 2004; Sprugel et al., 1991; Zwieniecki et al., 2003), elemental architectural modules (Hallé, 1986), differentially proliferating cell lineages (Klekowski, 1988; Otto & Hastings, 1998; White, 1979) and genomically differentiated mosaics (Pineda-Krch & Lehtilä, 2004b). The fusion of these kaleidoscopic perspectives on plant subindividuality with the idea that subindividual selection (i.e. among the different units that form the individual) and inheritance of somatic mutations can have evolutionary consequences (Buss, 1983a, 1983b; Otto & Hastings, 1998; Pineda-Krch & Fagerström, 1999; Pineda-Krch & Lehtilä, 2004a; Steele, 1979), provided conceptual grounds for a ‘genetic mosaicism hypothesis’ (GMH) of the ecology and evolution of plant variation (Whitham & Slobodchikoff, 1981; Whitham et al., 1984; Gill et al., 1995; Pineda-Krch & Lehtilä, 2004b; reviews in Herrera, 2009; Gerber, 2018).
Simplifying from Gill et al. (1995), the GMH rests on the simultaneous fulfilment of four central premises: (a) spontaneous mutations occur among the proliferating meristems; (b) the meristematic and modular basis of plant development assures that many of these mutations are preserved and expanded hierarchically among modules as the plant grows; (c) the differential growth and survival of ramets, branches and shoots should alter the genotypic configuration of the plant as it grows; and (d) intraplant trait heterogeneity arising from genotypic heterogeneity will affect individual fitness through effects on progeny traits, plant responses to the environment and/or responses of animal consumers (Herrera et al., 2021). Studies on wild plants have so far produced relatively few examples of spontaneous genetic mosaics within individuals and, whenever such mosaics have been identified, the estimated somatic mutation rates were extremely low and/or there was no evidence of extant or transgenerational phenotypic correlates of the genetic mosaicism (Cloutier et al., 2003; Gerber, 2018; Orr et al., 2020; Padovan et al., 2013; Ranade et al., 2015; Schmid-Siegert et al., 2017; Wang et al., 2019; but see Hanlon et al., 2019; Holeski et al., 2009). The proposal that genomically different parts of the same plant could contribute differentially to the next generation (i.e. differ in fitness) by virtue of their genomic distinctness is central to the GMH, but lack of empirical verification has probably hindered its acceptance in the long run despite strong theoretical foundations (Gerber, 2018; Herrera, 2009; Otto & Hastings, 1998; Pannell & Eppley, 2004; Pineda-Krch & Fagerström, 1999; Pineda-Krch & Lehtilä, 2004a).
Somatic mutations altering DNA sequences are not the only molecular mechanism with the capacity to produce stable genomic and phenotypic heterogeneity within individual plants. Potentially heritable epigenetic changes, such as those involving DNA cytosine methylation, also have the capacity to induce stable genomic heterogeneity and phenotypic variation within individual plants through their effects on gene expression, transposon activity, and plant growth and development (Cokus et al., 2008; Finnegan et al., 2000; Lister et al., 2008). This is supported by reports of homologous organs in different parts of the same genetic individual differing in extent and/or patterns of DNA methylation (Bian et al., 2013; Bitonti et al., 1996; Gao et al., 2010), and associations between subindividual epigenetic variation and intraplant phenotypic heterogeneity (Alonso et al., 2018; Herrera et al., 2019; Herrera & Bazaga, 2013; Marfil et al., 2009). Furthermore, persistent epigenetic mosaicism can arise within individuals of long-lived plants as a consequence of steady internal epigenetic diversification over lifetime (Herrera et al., 2021; Yao et al., 2021). These lines of evidence motivated Herrera et al.'s (2021) proposal of an ‘epigenetic mosaicism hypothesis’ (EMH) of plant variation consisting of the same elements (a)–(d) above as the original GMH but in which the terms ‘mutation’ and ‘genotype’ were replaced with ‘epimutation’ and ‘epigenotype’, respectively (see also Alonso et al., 2018; Herrera et al., 2019; for additional motivation). Support for the genealogical basis of epigenotypic mosaicism, and its dynamic nature over individuals' lifetimes (elements a–c), was recently provided by Herrera et al. (2021) for wild lavender (Lavandula latifolia Med., Lamiaceae). The objective of this paper is to further test on this species that extant intraplant epigenotypic variation has current and transgenerational phenotypic correlates which could eventually have ecological consequences by inducing fitness variations across different parts of the same individual and their respective offspring. Throughout this paper, ‘transgenerational’ will thus refer to the effects of maternal epigenetic mosaicism on phenotypic heterogeneity of offspring from the same maternal parent.
The following two questions will be specifically addressed in this study: (1) Does a predictable relationship exist between epigenotypic and phenotypic variation across different architecturally defined modules of the same L. latifolia shrub? and (2) Are the phenotypes of progenies produced by different modules of the same plant predictably related to the epigenotype of the module which produced the seeds, or in other words, Do epigenetically distinct plant parts produce phenotypically distinct progenies? The traits of maternal plants and progenies chosen for study were all directly or indirectly related to fecundity so that plausible inferences about fitness variations could be drawn from our results. To add strength to our conclusions, each of the preceding two questions will be addressed by considering epigenotypes and phenotypes of maternal plants and progenies from both multivariate (all traits considered simultaneously) and univariate (traits considered individually) perspectives. Our results show that modules of the same plant with different epigenotypes not only differ in extant traits, but they also predictably produce offspring which differ in fitness-related traits.
中文翻译：
植物内变异的生态意义：Lavandula latifolia 植物的表观遗传嵌合预测繁殖力相关性状的现存和跨代变异
1 简介
个体植物是非单一实体的概念至少可以追溯到伊拉斯谟·达尔文 (Erasmus Darwin，1800 ) 的工作，他强调“……一棵树的每个芽都是一个单独的植物；因此，一棵树就是一个家族或单个植物的群落”。最近，模块化植物生长所固有的内部多样性的生态、进化和生理影响已经从不同的角度并参考各种亚个体单位进行了相当详细的研究（Herrera， 2009）。后者包括，例如，生理上自主的部门（Orians & Jones, 2001 ; Watson, 1986 ; Watson & Casper, 1984)、分支和 ortostichies (Orians et al., 2004 ; Sprugel et al., 1991 ; Zwieniecki et al., 2003 )、基本结构模块 (Hallé, 1986 )、差异增殖细胞谱系 (Klekowski, 1988 ; Otto & Hastings, 1998 ; White, 1979 ) 和基因组分化马赛克 (Pineda-Krch & Lehtilä, 2004b )。这些关于植物亚个体的万花筒观点与亚个体选择（即在形成个体的不同单位之间）和体细胞突变的遗传可以产生进化后果的观点相融合（Buss， 1983a，1983b; 奥托和黑斯廷斯， 1998 年；Pineda-Krch 和 Fagerström， 1999 年；Pineda-Krch & Lehtilä， 2004a；Steele， 1979 年），为植物变异的生态学和进化的“遗传镶嵌假说”（GMH）提供了概念基础（Whitham 和 Slobodchikoff， 1981 年；Whitham 等人， 1984 年；Gill 等人， 1995 年；Pineda-Krch & Lehtilä， 2004b；Herrera 评论， 2009 年；Gerber， 2018 年）。
从 Gill 等人简化。（1995 年），GMH 依赖于同时满足四个中心前提：（a）自发突变发生在增殖的分生组织中；(b) 植物发育的分生组织和模块基础确保了这些突变中的许多在植物生长时在模块之间分层保存和扩展；(c) 分株、枝条和枝条的不同生长和存活应随着植物的生长而改变其基因型构型；(d) 由基因型异质性引起的植物内性状异质性将通过影响后代性状、植物对环境的反应和/或动物消费者的反应来影响个体适应性（Herrera 等， 2021）。迄今为止，对野生植物的研究在个体中产生的自发遗传嵌合体的例子相对较少，每当发现这种嵌合体时，估计的体细胞突变率极低和/或没有证据表明遗传基因的现存或跨代表型相关性。镶嵌现象（Cloutier 等人， 2003 年；Gerber 等人， 2018 年；Orr 等人， 2020 年；Padovan 等人， 2013 年；Ranade 等人， 2015 年；Schmid-Siegert 等人， 2017 年；Wang 等人， 2019 年；但请参见 Hanlon 等人， 2019 年；Holeski 等人， 2009 年）。同一植物的基因组不同部分可能因其基因组独特性而对下一代有不同的贡献（即适应性不同），这一提议是 GMH 的核心，但缺乏经验验证可能阻碍了它在长期内的接受，尽管坚实的理论基础（Gerber， 2018；Herrera， 2009；Otto & Hastings， 1998；Pannell & Eppley， 2004；Pineda-Krch & Fagerström， 1999；Pineda-Krch & Lehtilä， 2004a）。
改变 DNA 序列的体细胞突变并不是唯一能够在单个植物中产生稳定的基因组和表型异质性的分子机制。潜在可遗传的表观遗传变化，例如那些涉及 DNA 胞嘧啶甲基化的变化，也有能力通过其对基因表达、转座子活性和植物生长发育的影响在个体植物内诱导稳定的基因组异质性和表型变异 (Cokus et al., 2008 ) ；Finnegan 等人， 2000 年；Lister 等人， 2008 年）。同一遗传个体不同部位的同源器官的 DNA 甲基化程度和/或模式不同的报道支持了这一点（Bian 等人， 2013；Bitonti 等人， 1996；Gao 等人， 2010 年），以及亚个体表观遗传变异与植物内表型异质性之间的关联（Alonso 等人， 2018 年；Herrera 等人， 2019 年；Herrera & Bazaga， 2013 年；Marfil 等人， 2009 年）。此外，由于在整个生命周期内稳定的内部表观遗传多样化，长寿植物的个体中可能会出现持久的表观遗传嵌合现象（Herrera 等人， 2021 年；Yao 等人， 2021 年）。这些证据促使 Herrera 等人 ( 2021) 提出植物变异的“表观遗传嵌合假说”（EMH），由与上述原始 GMH 相同的元素 (a)-(d) 组成，但其中术语“突变”和“基因型”被“表观突变”取代和“表观基因型”（另见 Alonso 等人， 2018 年；Herrera 等人， 2019 年；其他动机）。Herrera 等人最近提供了对表观基因型嵌合体的谱系学基础及其在个体一生中的动态性质（元素 a-c）的支持。( 2021 ) 野生薰衣草 ( Lavandula latifolia )医学，唇形科）。本文的目的是进一步测试该物种，即现存的植物内表观基因型变异具有当前和跨代表型相关性，这些相关性最终可能通过诱导同一个体及其各自后代不同部位的适应度变化而产生生态后果。因此，在整篇论文中，“跨代”将指母体表观遗传嵌合体对来自同一母本的后代表型异质性的影响。
本研究将具体解决以下两个问题：(1) 相同L. latifolia的不同结构定义模块的表观基因型和表型变异之间是否存在可预测的关系灌木？(2) 同一植物的不同模块产生的后代表型是否与产生种子的模块的表观基因型相关，或者换句话说，表观遗传不同的植物部分是否产生表型不同的后代？选择用于研究的母系植物和后代的性状都与繁殖力直接或间接相关，因此可以从我们的结果中得出关于适应性变化的合理推论。为了加强我们的结论，前面两个问题中的每一个都将通过从多变量（同时考虑所有性状）和单变量（单独考虑性状）的角度考虑母本植物和后代的表观基因型和表型来解决。
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